Neural Correlates of Crowding in Macaque Area V4

J Neurosci. 2024 Jun 12;44(24):e2260232024. doi: 10.1523/JNEUROSCI.2260-23.2024.

Abstract

Visual crowding refers to the phenomenon where a target object that is easily identifiable in isolation becomes difficult to recognize when surrounded by other stimuli (distractors). Many psychophysical studies have investigated this phenomenon and proposed alternative models for the underlying mechanisms. One prominent hypothesis, albeit with mixed psychophysical support, posits that crowding arises from the loss of information due to pooled encoding of features from target and distractor stimuli in the early stages of cortical visual processing. However, neurophysiological studies have not rigorously tested this hypothesis. We studied the responses of single neurons in macaque (one male, one female) area V4, an intermediate stage of the object-processing pathway, to parametrically designed crowded displays and texture statistics-matched metameric counterparts. Our investigations reveal striking parallels between how crowding parameters-number, distance, and position of distractors-influence human psychophysical performance and V4 shape selectivity. Importantly, we also found that enhancing the salience of a target stimulus could alleviate crowding effects in highly cluttered scenes, and this could be temporally protracted reflecting a dynamical process. Thus, a pooled encoding of nearby stimuli cannot explain the observed responses, and we propose an alternative model where V4 neurons preferentially encode salient stimuli in crowded displays. Overall, we conclude that the magnitude of crowding effects is determined not just by the number of distractors and target-distractor separation but also by the relative salience of targets versus distractors based on their feature attributes-the similarity of distractors and the contrast between target and distractor stimuli.

Keywords: object recognition; primate; saliency computation; shape perception; temporal dynamics; ventral visual pathway.

MeSH terms

  • Animals
  • Female
  • Humans
  • Macaca mulatta*
  • Male
  • Neurons* / physiology
  • Pattern Recognition, Visual / physiology
  • Photic Stimulation* / methods
  • Psychophysics
  • Visual Cortex* / physiology